ORIGINALARTICLE

Biogeographical assessment ofmyxomycete assemblages fromNeotropical and Asian PalaeotropicalforestsNikki Heherson A. Dagamac1* , Yuri K. Novozhilov2,3,

Steven L. Stephenson4, Carlos Lado5, Carlos Rojas6,

Thomas Edison E. dela Cruz7, Martin Unterseher1 and Martin Schnittler1

1Institute of Botany and Landscape Ecology,

Ernst Moritz Arndt University Greifswald,

Soldmannstr. 15, D-17487 Greifswald,

Germany, 2Laboratory of Systematics and

Geography of Fungi, Komarov Botanical

Institute of the Russian Academy of Sciences,

Prof. Popov Street 2, 197376 St. Petersburg,

Russia, 3Joint Russian-Vietnamese Tropical

Research and Technological Centre of the

A.N. Severtsov Institute of Ecology and

Evolution RAS, South Branch 3, Street 3/2,

10 District, Ho Chi Minh City, Vietnam,4Department of Biological Sciences, University

of Arkansas, Fayetteville, AR 72701, USA,5Real Jard�ın Bot�anico, CSIC, Plaza de

Murillo 2, 28014 Madrid, Spain, 6Engineering

Research Institute and Department of

Agricultural Engineering, University of Costa

Rica, San Pedro de Montes de Oca 11501,

Costa Rica, 7Department of Biological

Sciences, University of Santo Tomas, Espa~na,

1015 Manila, Philippines

*Correspondence: Nikki Heherson A.

Dagamac, Institute of Botany and Landscape

Ecology, Ernst Moritz Arndt University

Greifswald, Soldmannstr. 15, D-17487

Greifswald, Germany.

E-mail: nhadagamac@gmail.com

ABSTRACT

Aim Lowland/highland and Neotropical/Asian Palaeotropical assemblages of

myxomycetes were compared to test the null hypothesis that neither species

diversity nor species composition differs between the two ecoregions. This can

be expected if myxomycetes behave as ubiquists and are capable of unlimited

long distance dispersal.

Location Four pairs (lowland/highland) of comprehensive regional surveys

encompassing c. 7500 specimens were compared; these represented Neotropical

(Yasuni/Maquipucuna in Ecuador; Guanacaste/Monteverde in Costa Rica) and

Asian Palaeotropical forests (Cat Tien/Bi Dup Nui Ba in Vietnam; Chiang Mai

in Thailand/South Luzon in the Philippines).

Methods Each survey was carried out in an area characterized by relatively

homogenous vegetation consisting of natural or near-natural forests, and incor-

porated both field collecting and the use of moist chamber cultures, and all

observed fructifications were recorded. Analyses of diversity (i.e. richness) and

community composition were carried out with EstimateS and R.

Results Between 400 and 2500 records per survey were obtained. Species accu-

mulation curves indicated moderate to nearly exhaustive completeness (70–94% of expected species richness recorded). Multivariate analyses suggest that

geographical separation (Neotropic versus Palaeotropic) explained the observed

differences in composition of myxomycete assemblages better than habitat

differences (lowland versus highland forests).

Main Conclusion Both geographically restricted morphospecies and differ-

ences in myxomycete assemblages provide evidence that myxomycetes are not

ubiquists but tend to follow the moderate endemicity hypothesis of protist

biogeography.

Keywords

Amoebozoa, community ecology, dispersal barriers, endemicity, morphos-

pecies, myxomycete, plasmodial slime moulds

INTRODUCTION

Myxomycetes (plasmodial slime moulds) are one of the few

protist groups that can be studied in the field, based on their

above-ground macroscopic fructifications which release air-

borne spores (Schnittler et al., 2012). Most of our knowledge

about myxomycete assemblages has been derived from sur-

veys which have recorded fructifications in the field or from

moist chamber cultures (Stephenson et al., 2008). In terms

of biogeography, most studies have been carried out in tem-

perate regions of the Northern Hemisphere, including alpine

and subalpine mountains (Ronikier & Ronikier, 2009;

Novozhilov et al., 2013), tundra (Novozhilov et al., 1999;

Stephenson et al., 2000), winter-cold deserts (Schnittler &

Novozhilov, 2000; Schnittler, 2001; Novozhilov & Schnittler,

2008) and temperate grasslands (Rollins & Stephenson,

2013). Only recently have other parts of the world, such as

tropical zones, warm deserts or the Patagonian steppe been

1524 http://wileyonlinelibrary.com/journal/jbi ª 2017 John Wiley & Sons Ltddoi:10.1111/jbi.12985

Journal of Biogeography (J. Biogeogr.) (2017) 44, 1524–1536

studied systematically (Estrada-Torres et al., 2009; Wrigley

de Basanta et al., 2010; Lado et al., 2013, 2014, 2016). At the

level of morphologically recognizable taxa, many myx-

omycete species display cross-continental distribution pat-

terns (Stephenson et al., 2008). Even remote islands such as

the Galapagos Islands (Eliasson & Nannenga-Bremekamp,

1983), the Hawaiian archipelago (Eliasson, 1991), Macquarie

Island (Stephenson et al., 2007) or Bohol Island (Macabago

et al., 2017) do not seem to have endemic taxa present.

In contrast, numerous myxomycete species described

within the last few decades (Schnittler & Mitchell, 2000) are

known from only one or a few localities. Moreover, certain

vegetation types contain species that are locally abundant but

do not occur elsewhere. This is best documented for deserts;

examples include Physarum pseudonotabile Novozh., Schnit-

tler & Okun in Central Asia (Novozhilov & Schnittler, 2008;

Novozhilov et al., 2013), or Perichaena calongei Lado, D.

Wrigley & Estrada, Didymium infundibuliforme D. Wrigley,

Lado & Estrada and Physarum atacamense D. Wrigley, Lado

& Estrada in South America (Lado et al., 2009; Wrigley de

Basanta et al., 2009, 2012; Araujo et al., 2015). Whether this

is due to the lack of data from many areas of the world or

due to some morphologically recognizable myxomycete spe-

cies occurring with a limited distribution is a question being

debated. In spite of their capability for long distance disper-

sal via spores (Kamono et al., 2009), it seems that in keeping

with other eukaryotic protists such as testate amoebae, cili-

ates and diatoms (Foissner, 2006, 2008), myxomycetes may

support the moderate endemicity hypothesis (Foissner, 1999)

for protist biogeography. This hypothesis recognizes that cos-

mopolitan species of protists may exist in nature but due to

geographical barriers, about 30% of all species can show geo-

graphically restricted distributions.

Various studies have reported species of myxomycetes

fruiting predominantly in specific vegetation types (Schnittler

& Stephenson, 2000), on particular substrates (Wrigley de

Basanta et al., 2008; Tucker et al., 2011), or during certain

seasons (Rojas & Stephenson, 2007; Dagamac et al., 2012).

The unresolved question is whether such differences are

entirely the result of microhabitat preferences (wherever suit-

able substrata occur under suitable microclimatic conditions,

the respective species will fruit), as suggested for Barbeyella

minutissima Meyl. (Schnittler et al., 2000). If microhabitat

suitability represents the only factor determining occurrence,

effective long-distance dispersal or persistent populations of

amoebae must be assumed. Indeed, 18S rRNA gene

sequences of the commonly highland fruiting nivicolous

genus Meriderma were already detected in lowland regions,

indicating persistence (presumably of amoebae) where this

taxon never fruits (Fiore-Donno et al., 2016). Furthermore,

another explanation is to assume the existence of barriers to

distribution, at least between continents (Estrada-Torres

et al., 2013; Aguilar et al., 2014). Long-distance dispersal has

been reported for myxomycetes (Kamono et al., 2009), and

the patchy occurrence of nivicolous myxomycetes in moun-

tain ranges of the Northern and Southern Hemispheres

corroborates this (Ronikier & Lado, 2015). Thus, transconti-

nental dispersal events may happen, but it is unknown if the

frequency of gene flow mediated by spore dispersal is suffi-

cient to prevent allopatric speciation from occurring between

transcontinental populations. As has been shown for the

much better documented ferns and fern allies (usually pos-

sessing much larger spores), species may show transcontinen-

tal distribution patterns or may be restricted to one

continent only (Karst et al., 2005).

An adequate ‘field laboratory’ to address the question of

myxomycetes distribution would be a major ecosystem that

is stable for a long period of time and is globally distributed

– in other words, tropical regions covered naturally by rain

forests. For myxomycetes, many diversity assessments have

been carried out in Neotropical forests. These range from

country checklists (Brazil, Cavalcanti, 2010; Colombia, Rojas

et al., 2012a; Costa Rica, Rojas et al., 2010; El Salvador,

Rojas et al., 2013) to abundance-based diversity assessments

of natural habitats (Lado et al., 2003; Rojas & Stephenson,

2012). About half of the c. 1000 known morphospecies of

myxomycetes (Lado, 2005–2016) have been recorded from

the Neotropics (Lado & Wrigley de Basanta, 2008). Our

knowledge of myxomycete diversity of the Asian Palaeotrop-

ics is more limited, and c. 200 taxa are known. Nevertheless,

several investigations have been carried out in lowland and

montane vegetation types of Southeast Asia, including Thai-

land (Tran et al., 2008; KoKo et al., 2010), Singapore (Ros-

ing et al., 2011), Laos (KoKo et al., 2012), Vietnam

(Novozhilov & Mitchell, 2014; Novozhilov et al., 2014; Tran

et al., 2014; Novozhilov & Stephenson, 2015) and the Philip-

pines (Dagamac et al., 2015a,b, 2017).

This study compared myxomycete assemblages between

Neotropical and Asian Palaeotropical forests with the objec-

tive of answering several questions: First, are there differences

in species composition and/or species abundance between

(1) different vegetation types within a particular region

(tropical lowland versus highland forests) or (2) comparable

vegetation types on different continents (Asian Palaeotropics:

Thailand, Philippines and Vietnam versus Neotropics: Costa

Rica and Ecuador)? Second, are there species apparently

restricted to only one of the regions in question? Third, does

a comparison of regional survey data provide evidence to

support the ‘moderate endemicity’ hypothesis (Foissner,

2006) for eukaryotic protists?

MATERIALS AND METHODS

Compilation of regional datasets

A double-paired design (four Neotropical and four Asian

Palaeotropical/four lowland and four highland areas, Fig. 1,

Table 1) was chosen to identify differences in species compo-

sition and abundance associated with geography and/or ele-

vation as a proxy for habitat type. Five criteria were applied

to select the eight datasets used in this study. (1) The area

for each survey should be relatively homogenous for a major

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Biogeographical assessment of myxomycete assemblages across the Tropics

forest type. (2) The two components of a survey should

include at least 100 records from the field collections plus

100 records obtained by the moist chamber culture tech-

nique, with all major substrata (bark, aerial and ground lit-

ter) roughly equally represented. (3) Records should include

all fructifications observed in the field or in cultures, which

may be determined on the spot or collected for later deter-

mination. This allowed abundance estimates to be compiled

for all of the species present, but excluded many published

studies which provided only pure species lists without abun-

dance data. (4) The exhaustiveness of a survey should exceed

70% in order to recover the majority of species likely to

occur in a particular region. In a strict sense, this could not

be verified. As a proxy criterion, we checked if the Chao1

estimator for an individual-based accumulation curve (in-

cluding all records from each survey) converged (standard

deviation should not monotonously increase but decrease

with increasing number of records) and if its final value

Figure 1 World map showing the eight areas surveyed for myxomycetes that were used in this study, the number of records found andthe total number of species accounted on each survey. [Colour figure can be viewed at wileyonlinelibrary.com]

Table 1 Characteristics of the eight investigated areas in the Neotropical and Asian Palaeotropics; naming the investigated area,

literature references, elevation and geographical coordinates, the number of moist chamber cultures prepared and vegetation types,applying by Holdridge et al. (1971) classification of tropical forests. Surveys are listed in the sequence Neotropical/Palaeotropical (N/P)

and lowland/highland (L/H) for each region.

Region Reference

Elevation

(m a.s.l.) Location

Moist chamber

cultures Vegetation type

NL: Costa Rica,

Guanacaste

Schnittler & Stephenson

(2000)

10–300 08°470–10°580 N82°490–85°560 W

476 Tropical dry forest (excluding

volcano Cacao)

NL: Ecuador,

Yasuni

Lado et al. (2017) 200–275 04°000–04°040 N76°220–76°250 W

225 Tropical moist forest, Amazonian

lowland forest

NH: Costa Rica,

Monteverde

Rojas et al. (2010) 1000–1500 10°160–10°190 N84°440–84°480 W

c. 700 Tropical montane wet forest

NH: Ecuador,

Maquipucuna

Schnittler et al. (2002),

Stephenson et al. (2004a)

1250–2720 03°150–07°280 N78°340–78°280 W

475 Tropical montane wet forest

PL: Philippines,

South Luzon

Dagamac et al. (2017, 2015b) 10–524 12°750–14°100 0N120°540–124°090 E

1500 Tropical moist forest

PL: Vietnam, Cat

Tien

Novozhilov et al. (2017) 72–247 11°160–11°270 N107°030–107°260 E

954 Tropical moist forest

PH: Thailand,

Chiang Mai

Dagamac, N.H.A., Unterseher, M. &

Schnittler, M., unpublished

data; Rojas et al. (2012b),

KoKo et al. (2010);

900–2500 18°480–20°100 N98°290–99°720 E

c. 1000 Tropical montane wet forest

PH: Vietnam, Bi

Dup Nui Ba

Novozhilov, personal

communication

1375–1747 12°070–12°110 N108°380–108°420 E

922 Tropical montane wet forest

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N. H. A. Dagamac et al.

indicated a completeness of at least 70% (ratio observed to

expected species). (5) The habitats studied within a survey

should include at least pockets of natural or near-natural for-

ests, to reflect the natural species inventory to a significant

degree.

Moist chamber cultures and specimen determination

Moist chamber cultures were prepared in 9 cm Petri dishes

using standard procedures (e.g. Schnittler, 2001), incubated

under ambient light at room temperature (c. 20–24 °C) for

up to 90 days and checked regularly on at least five occa-

sions. To maintain moisture, distilled water was added over

the first 6 weeks of the incubation period. Mature fructifica-

tions were transferred to herbarium boxes, with one record

defined as a colony of fructifications from a single taxon

developing in one culture. Myxomycete taxa were deter-

mined according to morphological characters of the fructifi-

cations, using standard monographs of the group (e.g.

Nannenga-Bremekamp, 1967, 1991; Martin & Alexopoulos,

1969; Farr, 1976; Neubert et al., 1995–2000; Lado & Pando,

1997; Poulain et al., 2011) and public repositories (Eumyce-

tozoan Project at http://slimemold.uark.edu/; Discover Life at

http://www.discoverlife.org). Nomenclature follows Lado

(2005–2016). Voucher specimens are deposited in the

herbarium of the University of Arkansas (UARK), the Botan-

ical State Collection Munich (M), the herbarium of the

University of Costa Rica at San Jose (USJ), the Real Jard�ın

Bot�anico de Madrid, (MA-fungi), the University of Santo

Tomas, Manila (USTH) and the Komarov Botanical Institute

(LE).

Data analysis

Individual-based species accumulation curves were con-

structed for each study area using EstimateS 9.1 (Colwell,

2013, 100 randomizations). In accordance with Unterseher

et al. (2008), first a non-parametric estimator was calculated

using the ‘default settings’ of EstimateS (Chao1, Chao et al.,

2005); second species accumulation curves were fitted with

the hyperbolic function y = ax/(b + x), with the parameter a

providing an estimate for species richness. Myxomycete

abundance was classified according to the ACOR scale of

Stephenson et al. (1993), based upon the proportion of a

species to the total number of records for each survey: R–rare (< 0.5%), O–occasional (> 0.5–1.5%), C–common

(> 1.5–3%), A–abundant (> 3%). Abundance-based datasets

from each of the eight study areas (see Appendix S2 in Sup-

porting Information) and environmental variables (geograph-

ical region and elevation, Table 1) were analysed in R (R

Core Team, 2015). Diversity between the geographical

regions (Neotropics versus Palaeotropics) and habitats (low-

land versus highland) was compared using the classical rich-

ness indices of Fisher’s alpha, the Shannon index (considers

richness and evenness) and the first three numbers of Hill’s

diversity series (Hill, 1973; Morris et al., 2014); differences

were tested for significance by a Wilcoxon test. In addition,

the most probable abundance distribution model was deter-

mined from rank-abundance plots (Whittaker, 1965) testing

five models following Wilson (1991): Null (fits the broken

stick model), Preemption (fits the geometric series or Moto-

mura model), log-Normal, Zipf and Mandelbrot. Both diver-

sity indices and distribution models were calculated in the

‘vegan’ package of R, using the functions renyi and radfit,

respectively. Community composition between geography

and elevation was examined using (1) clustering analysis and

non-metric multidimensional scaling (NMDS) based on Bray

Curtis distances and (2) the statistical test PERMANOVA

based on 999 permutations using the functions hclust,

metaMDS and adonis of R (see Appendix S3 for input files).

RESULTS

Basic data, sampling intensity and species

composition

Altogether, the surveys from eight areas (Table 1, see Fig. S3

in Appendix S1) included a total of 7585 myxomycete

records (2844 from Neotropical and 4741 from Asian

Palaeotropical forests). A total of 239 taxa (species and vari-

eties) were recorded. Neotropical forests were less diverse

(150 taxa) than Asian Palaeotropical forests (196 taxa, see

Appendix S2 for a collated list). This difference remained if

the rarefied values (based on the lower number of 2844

records) from an analysis of the species accumulation curves

were considered: 150.0 vs. 172.8 taxa.

On both continents, numerous taxa were represented by

only one record (singleton) for the entire region (Neotropics:

40 taxa, 27% of all taxa; Palaeotropics: 43 taxa, 22%). The

eight surveys were between 70% and 88% complete accord-

ing to the Chao1 estimator, and between 76% and 94%

according to a hyperbolic regression (Table 2, see Fig. S1 in

Appendix S1). If the degree of exhaustiveness was estimated

by a hyperbolic function y = ax/(b + x), the fit was better

(R = 0.885, a = 97.3, P < 0.0001) than for the final values of

the Chao1 estimator (R = 0.716, a = 94.3, P < 0.0001,

Fig. 2). Even for the South Luzon survey that had the highest

number of records, the survey was no more than 91%

(Chao1) and 94% (hyperbolic regression) complete. With

increasing sampling effort the number of singleton species

declined (linear regression y = ax + b for a scatter plot of

records per survey versus number of singleton species:

R = 0.676, a = �0.0077, P = 0.0066).

According to the ACOR scale, 72% of all taxa in the four

Neotropical surveys (pooled to a common species list, see

Appendix S2 and Fig S2 in Appendix S1) were rare, 17%

were occasional, 7% were common and 5% were abundant.

In spite of being represented by 1.7 times more records, 80%

of all taxa from the Asian Palaeotropical surveys were rare,

7% were occasional, 11% were common and only 3% were

abundant. The five most abundant species in the Neotropical

forest were Didymium iridis (211 records), Didymium

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Biogeographical assessment of myxomycete assemblages across the Tropics

squamulosum (194), Physarum compressum (190), the dwarf

form of Arcyria cinerea (172, described in Schnittler, 2000)

and Hemitrichia calyculata (119). In the Asian Palaeotropical

forests, the list was headed by Arcyria cinerea (933), Didy-

mium squamulosum (194), Perichaena depressa (155), Cri-

braria microcarpa (149) and Diderma hemisphaericum (144).

Non-metric multidimensional scaling ordinations display

contrasting signals of species turnover for geographical

(Neotropical versus Asian Palaeotropical) and elevational

(lowland versus highland) differences. Species composition

of Neotropical forests differed significantly from that of

Asian Palaeotropical forests (R2 = 0.278, P = 0.088); disper-

sion ellipses of the two assemblages in NMDS did not over-

lap (Fig. 3a). Cluster analysis using Bray Curtis dissimilarity

(Fig. 3c) confirmed this bipartition. In contrast, there is no

significant difference between lowland and highland sample

groups (Fig. 3b, R2 = 0.117, P = 0.474).

Species abundance distribution and diversity

The rank-abundance plots tested for different abundance dis-

tribution models showed comparable results for Neotropical

and Asian Palaeotropical forests. For datasets pooled for the

two different geographical regions, log-Normal was the best

fitting model; for the comparison of lowlands versus high-

lands the log-Normal model best fit for the former and Man-

delbrot model provided a slightly better fit for the latter

(Fig. 4). Boxplots for several estimators of species diversity

(Fig. 5) were not always higher for the Palaeotropics

(Fig. 5a), as would be expected from a comparison of species

richness. The trend for elevational differences is clearer, since

all five indices were higher for lowland than for highland for-

ests (Fig. 5b). However, none of these differences was signifi-

cant (comparison between lowland and highland areas, see

Table S1 of Appendix S1, P > 0.05; between Neotropical and

Table 2 Statistical analysis of individual-based species accumulation curves of myxomycetes for the eight regional surveys in the tropics

(giving the area by name and classified as L = lowland, H = highland), showing numbers of records (Rec), species (Sp), rarified species(SpR), and values for numbers of species to expect according to the Chao1 estimator (mean � SD) and a fit with a hyperbolic function

y = ax/(b + x), with a as the estimator for the number of species to be expected. The per cent values denote the proportion of speciesfound on the number of species expected.

SurveyFound Expected: Chao1 Expected: Hyperbolic

Area Rec Sp SpR Chao1 SD % a SD R %

NL: Guanacaste 441 80 80.0 104.9 13.0 76.2 101.2 0.3 0.999 79.0

NL: Yasuni 924 92 75.8 126.5 19.3 72.8 103.2 0.2 0.996 89.2

NH: Monteverde 522 76 71.2 108.3 16.0 70.2 99.7 0.4 0.997 76.3

NH: Maquipucuna 957 85 66.1 105.8 10.9 80.3 97.7 0.3 0.992 87.0

PL: South Luzon 2045 80 57.1 86.0 4.7 93.0 85.6 0.1 0.994 93.5

PL: Cat Tien 1105 105 81.2 120.3 8.3 87.3 120.4 0.2 0.996 87.2

PH: Chiang Mai 1147 133 96.4 151.2 8.4 88.0 162.5 0.3 0.997 81.8

PH: Bi Dup Nui Ba 444 74 73.8 94.0 10.5 78.8 100.2 0.3 0.998 73.8

Figure 2 Relationship between the number of records and exhaustiveness of a survey (number of myxomycete species found as

proportion of the number of species to expect) for eight tropical surveys according to the Chao1 estimator � SD (a) and a hyperbolicregression (b). The values for eight regional surveys were in turn fitted with a hyperbolic function y = ax/(b + x), indicated as a solid

line with 95% confidence intervals as dotted lines. This fit results in estimates of the maximum exhaustiveness for an infinite number ofrecords of 94.2% (Chao1, R = 0.716) and 97.3% (hyperbolic regression, R = 0.885).

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

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N. H. A. Dagamac et al.

Asian Palaeotropical forests, P > 0.05). Similarly, species

richness was not higher in lowland forests, since rarefied

means were 73.5 � 11.2 for lowland and 76.9 � 13.4 for

highland areas (rarefied figures based on the lowest number

of 441 records for a survey, Table 2). This was caused by the

very high taxon number for one highland survey (northern

Thailand, 133 taxa, rarefied value 96.4).

DISCUSSION

Differences in species abundances and composition

between the Neotropics and Asian Palaeotropics

In recent years, abundance-based myxomycete data from the

Asian Palaeotropics have become available, allowing a com-

parison with Neotropical inventories. Almost all myxomycete

surveys revealed a high proportion of rare taxa, often found

only once in an area (e.g. Schnittler et al., 2002). To com-

pensate for the random component introduced by the rather

high proportion of rare species (between 15% and 38% of all

species in our surveys were represented by single records) we

considered only surveys recording species abundances. Four

pairs of large datasets were compiled to test the prima facie

null hypothesis that neither diversity nor species composition

differs between Neotropical and Asian Palaeotropical forests.

Given that similar macroecological conditions exist between

regions, this can be expected if there is efficient long-distance

dispersal by spores.

For a regional survey, there was some degree of hetero-

geneity in targeted microhabitats and/or substrata. Even for

large datasets, such as that from South Luzon, the number of

species recorded was lower than the number of expected spe-

cies. This was predicted to be the case even for infinitely

large surveys, as indicated by final percentages of 92% (esti-

mated via analysis of species accumulation curves based on

the Chao1 estimator) and 97% (hyperbolic regression, Fig. 2)

and a higher sampling effort seems to reduce the proportion

of rare species for a survey. These results reflected the

unavoidable degree of heterogeneity for surveys covering a

larger area. Nevertheless, the species accumulation curves

generated for the eight study areas suggest that the sampling

effort was sufficient to recover most of the species that are

realistically possible to recover.

Asian Palaeotropic forests seemed to be richer in species of

myxomycetes than Neotropic forests (rarefied species num-

bers: 172.8 vs. 150.0). The presence of conifers (Pinus spp.)

with acidic bark and wood in the mountains of Vietnam (Bi

Dup Nui Ba) and Thailand (Chiang Mai) may contribute,

Figure 3 Non-metric multidimensional scaling (NMDS) of species occurrences for the eight surveys based on (a) geographic location and(b) elevational location. Black dots represent the position of myxomycete species in the ordination space. Coloured circles and squares

represent the regions/areas; coloured ellipses denote dispersion based on standard deviation of point scores. (c) Clustering analysis using BrayCurtis dissimilarity distance based on species composition (species and abundances). [Colour figure can be viewed at wileyonlinelibrary.com]

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

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Biogeographical assessment of myxomycete assemblages across the Tropics

since here several myxomycete taxa (Barbeyella minutissima

Meyl., Echinostelium brooksii Whitney, E. colliculosum Whitney

& Keller, Lamproderma columbinum (Pers.) Rostaf., Licea

kleistobolus Martin, Lindbladia tubulina Fr., Paradiacheopsis

rigida (Brandza) Nann.-Bremek., and Trichia persimilis Karst.)

were recorded that are known to be common in coniferous

forests in temperate zones. Neotropical highland regions

investigated in this study lack conifers, but these do occur,

together with some of the species of myxomycete mentioned

above, on the summits of Mexican volcanoes (Lado & Wrigley

de Basanta, 2008). In addition, northern Thailand (Chiang

Mai) yielded the highest number of species (133), and this was

the only dataset compiled from several researchers working

independently. For this area, we cannot avoid the possibility

that in a few cases a particular taxon was assigned to two dif-

ferent names, causing overestimation of species numbers. The

dataset from northern Thailand also contained the highest

proportion of rare species (69.2%); and the number of single-

ton species (33) was above average (23.5).

The higher species richness of Asian Palaeotropical forests

was not reflected by all of the computed diversity indices,

but all indices were consistently higher for lowland than for

highland forests (Fig. 5b). These differences were not

statistically significant (Wilcoxon test) but were in congru-

ence with observations that myxomycete diversity in tropical

forests decreases with increasing elevation (Schnittler &

Stephenson, 2000; Stephenson et al., 2004b; Rojas &

Stephenson, 2008). In constantly wet highland forests, myx-

omycetes seemed to utilize aerial litter, which dries out fas-

ter, more often than ground microhabitats (Schnittler &

Stephenson, 2000; Lado et al., 2003, 2017). Therefore, the

moisture regime, not elevation per se may be the driver of

differences in the abundance of fruiting bodies (Rojas et al.,

2016).

Interestingly, when we consider species composition, a

statistically significant difference was observed among myx-

omycete assemblages in relation to geography (Neotropics

versus Palaeotropics) but not in relation to habitat type

(lowland versus highland forests). As in fungal endophytes

(Langenfeld et al., 2013), soil protist assemblages (Foissner,

2007; Bates et al., 2013), and marine ciliates (Stock et al.,

2013), geographical location best explains the differences in

assemblage composition. A biogeographical study of myx-

omycetes that focused only on tropical highland forests

found a similar pattern: a cluster analysis separated myx-

omycete assemblages recorded from Thailand from those of

Figure 4 Rank abundance plots based onthe abundance of species for the (a, b)

geographical (Neotropics versusPalaeotropic) and (c, d) elevational

(Lowland versus Highland) gradient fittedwith five species distribution models. All

records from region or elevation (foursurveys each) were pooled. The model

showing the best fit is highlighted by a thickline. [Colour figure can be viewed at

wileyonlinelibrary.com]

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1530

N. H. A. Dagamac et al.

Figure 5 Box plot showing the comparison of five different diversity indices (Alpha = Fisher’s alpha; Shannon = Shannon’s H index;

N0 = species richness; N1 = exponent of Shannon diversity and N2 = inverse of Simpson) in relations to (a) geography and (b)elevation. Data from four study areas were pooled according to (a) geography (Neo- versus Palaeotropics) and (b) elevation (lowland

versus highland regions).

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

1531

Biogeographical assessment of myxomycete assemblages across the Tropics

the Americas (Rojas et al., 2012b). Although elevation deter-

mined habitat availability (Rojas et al., 2010; Dagamac et al.,

2014) and forest types (Novozhilov et al., 2000; Rojas et al.,

2011), the high overlap of species composition between

assemblages of lowland and highland areas showed that

myxomycetes seem to find in both elevations suitable

microhabitats for fruiting.

Are there myxomycetes restricted to the tropics?

Several species were found in a single survey or a pair of

surveys only. Comatricha spinispora Novozh. & Mitchell (26

records), Diderma pseudostestaceum Novozh. & Mitchell

(14), D. cattiense Novozh. & Mitchell (18) and Perichaena

echinolophospora Novozh. & Stephenson (4) were found only

in surveys conducted in Vietnam. Craterium paraguayense

(Speg.) G. Lister (4) and Lamproderma muscorum (Lev.)

Hagelst. (7) were reported exclusively from the Costa Rican

highlands (Monteverde) dataset and Diachea silvaepluvialis

Farr (6) was found exclusively in Ecuador (Yasuni). More

species were found exclusively in either the Neotropical (35)

or the Asian Palaeotropical region (68), of which 24 and 30

species, respectively, were singletons. For instance, Cera-

tiomyxa morchella Welden (45 records) and C. sphaeros-

perma Boedijn (24) were found only in the Neotropical

region; Physarum echinosporum Lister (55) and Cribraria

minutissima Schwein. (41) occurred exclusively in surveys

from the Asian Palaeotropical region. However, at this

point, we have to consider the low taxonomic resolution

provided by a morphological-based approach. All studies

that entered the ‘biospecies’ level via cultivation and com-

patibility experiments (Clark & Haskins, 2013) or via molec-

ular markers (Feng & Schnittler, 2015) found that a given

‘morphospecies’ comprised several putative biospecies (de-

fined as reproductively isolated units). A first local survey

based on fructifications with a full barcoding component

estimated the relationship between morphospecies and ribo-

types, the latter indicating the existence of different biospe-

cies, to be 1:2–10 (Feng & Schnittler, 2017). Therefore, a

cosmopolitan morphospecies such as Arcyria cinerea (Bull.)

Pers., is likely to consist of several biospecies (Clark et al.,

2002) if studied by molecular methods, and therefore puta-

tive biospecies may be more restricted in distribution. This

is not obvious when looking at distribution ranges of myx-

omycetes (see examples in Stephenson et al., 2008) since

many morphospecies appear to have large or even cos-

mopolitan ranges. In other words, as in the case of pyreno-

mycetous fungi (Vasilyeva & Stephenson, 2014), we should

expect at least some species to be restricted to certain

regions of the world.

Morphological-based surveys support moderate

endemicity for eukaryotic protist

Given the apparent rarity of fructifications for many myx-

omycetes (Stephenson, 2011), abundance data are important

to identify cases of moderate endemicity. Ceratiomyxa morch-

ella Welden (Neotropics) and Physarum echinosporum Lister

(Asian Palaeotropics) may be good examples, both represent-

ing unmistakable morphospecies that were common only in

one of the two regions. For this finding, we can assume that

despite intense surveys in similar tropical environments, geo-

graphical barriers between continents have played a role in

the apparent differences noted for species abundance and

composition. We can also expect that geographical differ-

ences found in this study will become more evident if large

datasets on molecular diversity become available for myx-

omycetes. In a related morphological-based approach,

Estrada-Torres et al. (2013) considered numerous environ-

mental factors and found that historical geography explained

best the distribution of myxomycete assemblages in the

Americas. Even if this study used presence/absence data only,

they similarly noted that some species (e.g. Diderma tehuaca-

nense Estrada, D. Wrigley & Lado and Perichaena stipitata

Lado, Estrada & D.Wrigley) were found exclusively in one

area.

In summary, biogeographic patterns of myxomycetes in

the tropics provided evidence that species composition is dif-

ferent and this is due to at least some morphologically recog-

nizable taxa that are indeed restricted to particular

geographical areas, some appeared to be regionally or locally

endemic, and thus we may expect moderate endemicity to be

the rule rather than the exception.

ACKNOWLEDGEMENTS

N.H.A.D. acknowledges the German Academic Exchange

Service (DAAD) for a PhD scholarship. We are grateful to

Eva Heinrich, Melissa Pecundo, Arturo Estrada-Torres and

Diana Wrigley de Basanta for technical assistance with field

collecting and species determination. Y.K.N. was supported

by the scientific programs ‘Ecolan-1.2’ of the Russian-Viet-

namese Tropical Scientific and Technological Centre (Viet-

nam, Ho Chi Minh City) and a grant ‘Mycobiota of

southern Vietnam’, 01201255603 (Russia, St. Petersburg)

and is grateful to Ludmila A. Kartzeva (The Core Facility

Center ‘Cell and Molecular Technologies in Plant Science’

at the Komarov Botanical Institute RAS, St. Petersburg,

Russia) for the technical support (SEM). Surveys in the

Neotropics were enabled by several grants (DEB-9705464,

DEB-0102895 and DEB-0316284) from the National Science

Foundation and one grant (8890-11) from the National

Geographic Society to S.L.S. C.L. was funded by the US-

Spain Science and Technology Fulbright Cooperation Pro-

gram (Ref. 99075), and by the grant (CGL2014-52584P)

from the Spanish Government (Myxotropic project). C.R.

has been supported by University of Costa Rica through

research codes 731-B4-072 and 731-B5-062. T.E.D.C. was

supported by the Research Center for Natural and Applied

Sciences of University of Santo Tomas. M.U. acknowledges

financial support from the DAAD for his collection trip to

Thailand.

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

1532

N. H. A. Dagamac et al.

REFERENCES

Aguilar, M., Fiore-Donno, A.M., Lado, C. & Cavalier-Smith,

T. (2014) Using environmental niche models to test the

‘everything is everywhere’ hypothesis for Badhamia. The

ISME Journal, 8, 737–745.Araujo, J.C., Lado, C. & Xavier-Santos, S. (2015) Perichaena

calongei (Trichiales): a new record of Myxomycetes from

Brazil. Current Research in Environmental & Applied

Mycology, 5, 352–356.Bates, S.T., Clemente, J.C., Flores, G.E., Walters, W.A., Par-

frey, L.W., Knight, R. & Fierer, N. (2013) Global biogeog-

raphy of highly diverse protistan communities in soil. The

ISME Journal, 7, 652–659.Cavalcanti, L.H. (2010) Myxomycetes. Cat�alogo de plantas e

fungos do Brasil (ed. by R.C. Forzza, P.M. Leitman, A.

Costa et al.), vol. 1, pp. 94–104. Instituto de Pesquisas Jar-

dim Botanico do Rio de Janeiro, Rio de Janeiro.

Chao, A., Xhazdon, R.L., Colwell, R.K. & Shen, T.J. (2005) A

new statistical approach for assessing similarity of species

composition with incidence and abundance data. Ecology

Letters, 8, 148–159.Clark, J. & Haskins, E.F. (2013) The nuclear reproductive

cycle in the myxomycetes: a review. Mycosphere, 4, 233–248.

Clark, J., Schnittler, M. & Stephenson, S.L. (2002) Biosystem-

atics of the myxomycete Arcyria cinerea. Mycotaxon, 82,

343–346.Colwell, R.K. (2013) EstimateS: statistical estimation of species

richness and shared species from samples. Version 7. User’s

Guide and application. Available at: http://purl.oclc.org/es

timates (accessed 23 April 2014).

Dagamac, N.H.A., Stephenson, S.L. & dela Cruz, T.E.E.

(2012) Occurrence, distribution and diversity of myx-

omycetes (plasmodial slime molds) along two transects in

Mt. Arayat National Park, Pampanga, Philippines. Mycol-

ogy, 3, 119–126.Dagamac, N.H.A., Stephenson, S.L. & dela Cruz, T.E.E.

(2014) The occurrence of litter myxomycetes at different

elevations in Mt. Arayat, National Park, Pampanga, Philip-

pines. Nova Hedwigia, 98, 187–196.Dagamac, N.H.A., Rea-Maminta, M.A.D. & dela Cruz, T.E.E.

(2015a) Plasmodial slime molds of a tropical karst forest,

Quezon National Park, the Philippines. Pacific Science, 69,

407–418.Dagamac, N.H.A., Rea-Maminta, M.A.D., Batungbacal, N.S.,

Jung, S.H., Bulang, C.R.T., Cayago, A.G.R. & dela Cruz,

T.E.E. (2015b) Diversity of plasmodial slime molds (myx-

omycetes) on coastal, mountain, and community forests of

Puerto Galera, Oriental Mindoro, Philippines. Journal of

Asia Pacific Biodiversity, 8, 322–329.Dagamac, N.H.A., dela Cruz, T.E.E., Rea-Maninta, M.A.D.,

Aril-dela Cruz, J.V. & Schnittler, M. (2017) Rapid assess-

ment of myxomycete diversity in the Bicol Peninsula,

Philippines. Nova Hedwigia, 104, 31–46.

Eliasson, U. (1991) The myxomycete biota of the Hawaiian

Islands. Mycological Research, 95, 257–267.Eliasson, U. & Nannenga-Bremekamp, N.E. (1983) Myx-

omycetes from the Scalesia forest, Galapagos Islands. Pro-

ceedings of the Koninklijke Nederlandse Akademie van

Wetenschappen C, 86, 148–153.Estrada-Torres, A., Wrigley de Basanta, D., Conde, E. &

Lado, C. (2009) Myxomycetes associated with dryland

ecosystems of the Tehuac�an-Cuicatl�an Valley Biosphere

Reserve, Mexico. Fungal Diversity, 36, 17–56.Estrada-Torres, A., Wrigley de Basanta, D. & Lado, C. (2013)

Biogeographic patterns of the myxomycete biota of the

Americas using a parsimony analysis of endemicity. Fungal

Diversity, 59, 159–177.Farr, M.L. (1976) Flora Neotropica monograph no. 16 (Myx-

omycetes). New York Botanical Garden, New York.

Feng, Y. & Schnittler, M. (2015) Sex or no sex? Independent

marker genes and group I introns reveal the existence of

three sexual but reproductively isolated biospecies in Tri-

chia varia (Myxomycetes). Organisms Diversity & Evolu-

tion, 15, 631–650.Feng, Y. & Schnittler, M. (2017) Molecular or morphological

species? Myxomycete diversity in a deciduous forest of

northeastern Germany. Nova Hedwigia, 104, 359–380.Fiore-Donno, A.M., Weinert, J., Wubet, T. & Bonkowski, M.

(2016) Metacommunity analysis of amoeboid protists in

grassland soils. Scientific Reports, 6, 19068. doi:10.1028/

srep19068.

Foissner, W. (1999) Protist diversity: estimates of the near

imponderable. Protist, 150, 363–368.Foissner, W. (2006) Biogeography and dispersal of micro-

organisms: a review emphasizing protists. Acta Protozoolog-

ica, 45, 111–136.Foissner, W. (2007) Dispersal and biogeography of Protists:

recent advances. The Japanese Journal of Protozoology, 40,

1–16.Foissner, W. (2008) Protist diversity and distribution: some

basic considerations. Biodiversity and Conservation, 17,

235–242.Hill, M.O. (1973) Diversity and evenness: a unifying notation

and its consequences. Ecology, 54, 427–432.Holdridge, L.R., Grenke, W.C., Hatheway, W.H., Liang, T. &

Tosi, J.A., Jr (1971) Forest environments in tropical life

zones: a pilot study. Pergamon Press, Oxford, New York.

Kamono, A., Kojima, H., Matsumoto, J., Kawamura, K. &

Fukui, M. (2009) Airborne myxomycete spores: detection

using molecular techniques. Naturwissenschaften, 96, 147–151.

Karst, J., Gilbert, B. & Lechowicz, M.J. (2005) Fern com-

munity assembly: the roles of chance and the environ-

ment at a local and intermediate scales. Ecology, 86,

2473–2486.KoKo, T.W., Tran, H.T.M., Stephenson, S.L., Mitchell, D.W.,

Rojas, C., Hyde, K.D. & Lumyong, S. (2010) Myxomycetes

of Thailand. Sydowia, 62, 243–260.

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

1533

Biogeographical assessment of myxomycete assemblages across the Tropics

KoKo, T.W., Tran, H.T.M., Clayton, M.E. & Stephenson,

S.L. (2012) First records of myxomycetes in Laos. Nova

Hedwigia, 96, 73–81.Lado, C. (2005–2016) NomenMyx: an on line nomenclatural

information system of Eumycetozoa. Available at: http://www.

nomen.eumycetozoa.com (accessed 20 February 2015).

Lado, C. & Pando, F. (1997) Flora Mycologica Iberica, vol. 2.

Myxomycetes, I. Ceratiomyxales, Echinosteliales, Liceales,

Trichiales. J. Cramer & CSIC, Stuttgart.

Lado, C. & Wrigley de Basanta, D. (2008) A review of

Neotropical myxomycetes (1828–2008). Anales de Real

Jard�ın Bot�anico de Madrid, 65, 211–254.Lado, C., Estrada-Torres, A., Stephenson, S.L., Wrigley de

Basanta, D. & Schnittler, M. (2003) Biodiversity assess-

ment of myxomycetes from two tropical forest reserves in

Mexico. Fungal Diversity, 12, 67–110.Lado, C., Wrigley de Basanta, D., Estrada-Torres, A., Garc�ıa-

Carvajal, E., Aguilar, M. & Hern�andez, J.C. (2009)

Description of a new species of Perichaena (Myxomycetes)

from arid areas of Argentina. Anales del Jardin Bot�anico de

Madrid, 66, 63–70.Lado, C., Wrigley de Basanta, D., Estrada-Torres, A. &

Stephenson, S.L. (2013) The biodiversity of Myxomycetes

in Central Chile. Fungal Diversity, 59, 3–32.Lado, C., Wrigley de Basanta, D., Estrada-Torres, A. &

Garc�ıa-Carvajal, E. (2014) Myxomycete diversity of the

Patagonian Steppe and bordering areas in Argentina. Ana-

les del Jard�ın Bot�anico de Madrid, 71, 1–35.Lado, C., Wrigley de Basanta, D., Estrada-Torres, A. &

Stephenson, S.L. (2016) Myxomycete diversity in the

coastal desert of Peru with emphasis on the lomas forma-

tion. Anales del Jard�ın Bot�anico de Madrid, 73, e032.

Lado, C., Estrada-Torres, A., Wrigley de Basanta, D., Schnit-

tler, M. & Stephenson, S.L. (2017) A rapid biodiversity

assessment of myxomycetes from a primary tropical moist

forest of the Amazon basin in Ecuador. Nova Hedwigia,

104, 293–321.Langenfeld, A., Prado, S., Nay, B., Cruaud, C., Lacoste, S.,

Bury, E., Hachette, F., Hosoya, T. & Dupont, J. (2013)

Geographic locality greatly influences fungal endophyte

communities in Cephalotaxus harringtonia. Fungal Biology,

117, 124–136.Macabago, S.A.B., Dagamac, N.H.A., Dela Cruz, T.E.E. &

Stephenson, S.L. (2017) Implications of the role of dispersal

on the occurrence of litter-inhabiting myxomycetes in dif-

ferent vegetation types after a disturbance: a case study in

Bohol Islands, Philippines. Nova Hedwigia, 104, 221–236.Martin, G. & Alexopoulos, C.J. (1969) The Myxomycetes.

University of Iowa Press, Iowa.

Morris, E.K., Caruso, T., Buscot, F., Fischer, M., Hancock,

C., Maier, T.S., Meiners, T., M€uller, C., Obermaier, E.,

Prati, D., Socher, S.A., Sonnemann, I., W€aschke, N.,

Wubet, T., Wurst, S. & Rillig, M.C. (2014) Choosing and

using diversity indices: insights for ecological applications

from the German Biodiversity Exploratories. Ecology and

Evolution, 4, 3514–3524.

Nannenga-Bremekamp, N.E. (1967) Notes on Myxomycetes.

XII. A revision of the Stemonitales. Proceedings of the

Koninklijke Nederlandse Akademie Van Wetenschappen Ser.

C, 70, 201–216.Nannenga-Bremekamp, N.E. (1991) A guide to temperate

Myxomycetes. Biopress Limited, Bristol.

Neubert, H., Nowotny, W. & Baumann, K. (1995–2000) Die

Myxomyceten. Vol. 1–3. Karlheinz Baumann Verlag,

Gomaringen.

Novozhilov, Y.K. & Mitchell, D.W. (2014) A new spe-

cies of Comatricha (Myxomycetes) from southern

Vietnam. Novosti Sistematiki Nizshikh Rastenii, 48,

188–195.Novozhilov, Y.K. & Schnittler, M. (2008) Myxomycete diver-

sity and ecology in arid regions of the Great Lake Basin of

western Mongolia. Fungal Diversity, 30, 97–119.Novozhilov, Y.K. & Stephenson, S.L. (2015) A new species of

Perichaena (Myxomycetes) with reticulate spores from

southern Vietnam. Mycologia, 107, 137–141.Novozhilov, Y.K., Schnittler, M. & Stephenson, S.L. (1999)

Myxomycetes of the Taimar Peninsula (north-central

Siberia). Karstenia, 39, 77–97.Novozhilov, Y.K., Schnittler, M., Rollins, A.W. & Stephen-

son, S.L. (2000) Myxomycetes from different forest types

in Puerto Rico. Mycotaxon, 77, 285–299.Novozhilov, Y.K., Okun, M.V., Erastova, D.A., Shchepin,

O.N., Zemlyanskaya, I.V., Garc�ıa-Carvajal, E. & Schnittler,

M. (2013) Description, culture and phylogenetic position

of a new xerotolerant species of Physarum. Mycologia, 105,

1535–1546.Novozhilov, Y.K., Mitchell, D.W., Okun, M.V. & Shchepin,

O.N. (2014) New species of Diderma from Vietnam. Myco-

sphere, 5, 554–564.Novozhilov, Y.K., Erastova, D.A., Shchepin, O.N., Schnittler,

M., Alexandrova, A.V., Popov, E.S. & Kuznetzov, A.N.

(2017) Myxomycetes associated with monsoon lowland tall

tropical forests in southern Vietnam. Nova Hedwigia, 104,

143–182.Poulain, M., Meyer, M. & Bozonnet, J. (2011) Les Myxo-

mycètes. Guide de détermination, Fédération Mycologique

et Botanique Dauphiné-Savoie, Sévrier.R Core Team (2015) R: a language and environment for sta-

tistical computing. Available at: https://www.R-project.org

(accessed 18 October 2015).

Rojas, C. & Stephenson, S.L. (2007) Distribution and ecology

of myxomycetes in the high-elevation oak forests of Cerro

Bellavista, Costa Rica. Mycologia, 99, 534–543.Rojas, C. & Stephenson, S.L. (2008) Myxomycete ecology

along an elevational gradient on Cocos Island, Costa Rica.

Fungal Diversity, 29, 117–127.Rojas, C. & Stephenson, S.L. (2012) Rapid assessment of the

distribution of myxomycetes in a southwestern Amazon

forest. Fungal Ecology, 5, 726–733.Rojas, C., Schnittler, M. & Stephenson, S.L. (2010) A review

of the Costa Rican myxomycetes (Amebozoa). Brenesia,

73–74, 39–57.

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

1534

N. H. A. Dagamac et al.

Rojas, C., Stephenson, S.L. & Huxel, G. (2011) Macroecology

of high elevation myxomycete assemblages in the northern

Neotropics. Mycological Progress, 10, 423–437.Rojas, C., Herrera, N. & Stephenson, S.L. (2012a) An update

on the myxomycete biota (Amoebozoa: Myxogastria) of

Colombia. Check List, 8, 617–619.Rojas, C., Stephenson, S.L., Valverde, R. & Estrada-Torres, A.

(2012b) A biogeographical evaluation of high-elevation

myxomycete assemblages in the northern Neotropics. Fun-

gal Ecology, 5, 99–113.Rojas, C., Morales, R.E., Calder�on, I. & Clerc, P. (2013) First

records of myxomycetes from El Salvador. Mycosphere, 4,

1042–1051.Rojas, C., Valverde, R. & Calvo, E. (2016) Does elevation

influence the distributional patterns of tropical myx-

omycetes? A case study in Costa Rica. Mycology, 7, 45–52.Rollins, A.W. & Stephenson, S.L. (2013) Myxomycetes asso-

ciated with grasslands of the western central United States.

Fungal Diversity, 59, 147–158.Ronikier, A. & Lado, C. (2015) Nivicolous Stemonitales

(Myxomycetes) from the Austral Andes. Analysis of

morphological variability, distribution and phenology as a

first step towards testing the large-scale coherence of spe-

cies and biogeographical properties. Mycologia, 107, 258–283.

Ronikier, A. & Ronikier, M. (2009) How ‘alpine’ are nivi-

colous myxomycetes? A worldwide assessment of altitudi-

nal distribution. Mycologia, 101, 1–16.Rosing, W.C., Mitchell, D.W., Moreno, G. & Stephenson,

S.L. (2011) Addition to the myxomycetes of Singapore.

Pacific Science, 65, 391–400.Schnittler, M. (2000) Foliicolous liverworts as a microhabitat

for Neotropical Myxomycetes. Nova Hedwigia, 72, 259–270.Schnittler, M. (2001) Ecology of myxomycetes of a winter-

cold desert in western Kazakhstan. Mycologia, 93, 653–669.Schnittler, M. & Mitchell, D.W. (2000) Species diversity in

myxomycetes based on the morphological species concept

– a critical examination. Stapfia, 73, 55–61.Schnittler, M. & Novozhilov, Y.K. (2000) Myxomycetes of

the winter-cold desert in western Kazakhstan. Mycotaxon,

74, 267–285.Schnittler, M. & Stephenson, S.L. (2000) Myxomycete biodi-

versity in four different forest types in Costa Rica. Mycolo-

gia, 92, 626–637.Schnittler, M., Stephenson, S.L. & Novozhilov, Y.K. (2000)

Ecology and world distribution of Barbeyella minutissima

(Myxomycetes). Mycological Research, 104, 1518–1523.Schnittler, M., Lado, C. & Stephenson, S.L. (2002) Rapid

biodiversity assessment of a tropical myxomycete assem-

blage – Maquipucuna Cloud Forest Reserve, Ecuador. Fun-

gal Diversity, 9, 135–167.Schnittler, M., Novozhilov, Y.K., Romeralo, M., Brown, M.

& Spiegel, F.W. (2012) Myxomycetes and Myxomycete-like

organisms. Englers syllabus of plant families, vol. 4. (ed. by

W. Frey), pp. 12–88. Borntr€ager, Stuttgart.

Stephenson, S.L. (2011) From morphological to molecular:

studies of myxomycetes since the publication of the Mar-

tin and Alexopoulos monograph. Fungal Diversity, 50,

21–34.Stephenson, S.L., Kalyanasundaram, I. & Lakhanpal, T.N.

(1993) A comparative biogeographical study of myx-

omycetes in the mid-Appalachians of eastern North Amer-

ica and two regions of India. Journal of Biogeography, 20,

645–657.Stephenson, S.L., Novozhilov, Y.K. & Schnittler, M. (2000)

Distribution and ecology of myxomycetes in highlatitude

regions of the Northern Hemisphere. Journal of Biogeogra-

phy, 27, 741–754.Stephenson, S.L., Schnittler, M. & Lado, C. (2004a) Ecologi-

cal characterization of a tropical myxomycete assemblage –Maquipucuna Cloud Forest reserve, Ecuador. Mycologia,

96, 488–497.Stephenson, S.L., Schnittler, M., Lado, C., Estrada-Torres, A.,

Wrigley de Basanta, D., Landolt, J.C., Novozhilov, Y.K.,

Clark, J., Moore, D.L. & Spiegel, F.W. (2004b) Studies of

Neotropical myxomycetozoans. Systematic Geography of

Plants, 74, 87–108.Stephenson, S.L., Laursen, G.A. & Seppelt, R.D. (2007) Myx-

omycetes of subantarctic Macquarie Island. Australian

Journal of Botany, 55, 439–449.Stephenson, S.L., Schnittler, M. & Novozhilov, Y.K. (2008)

Myxomycete diversity and distribution from the fossil

record to the present. Biodiversity and Conservation, 17,

285–301.Stock, A., Edgcomb, V., Orsi, W., Filker, S., Breiner, H.W.,

Yakimov, M.M. & Stoeck, T. (2013) Evidence for isolated

evolution of deep sea ciliates communities through geolog-

ical separation and environmental selection. BMC Microbi-

ology, 13, 150. doi:10.1186/1471-2180-13-150.

Tran, D.Q., Nguyen, H.T.N., Tran, H.T.M. & Stephenson,

S.L. (2014) Myxomycetes from three lowland tropical for-

ests in Vietnam. Mycosphere, 5, 662–672.Tran, H.T.M., Stephenson, S.L., Hyde, K.D. & Mongkolporn,

O. (2008) Distribution and occurrence of myxomycetes on

agricultural ground litter and forest floor litter in Thai-

land. Mycologia, 100, 181–190.Tucker, D.R., Coelho, I.L. & Stephenson, S.L. (2011) House-

hold slime molds. Nova Hedwigia, 93, 177–182.Unterseher, M., Schnittler, M., Dormann, C. & Sickert, A.

(2008) Application of species richness estimators for the

assessment of fungal diversity. FEMS Microbiology Letters,

282, 205–213.Vasilyeva, L.N. & Stephenson, S.L. (2014) Biogeographical

patterns in pyrenomycetous fungi and their taxonomy. 4.

Hypoxylon and the southern United States. Mycotaxon,

129, 85–95.Whittaker, R.H. (1965) Dominance and diversity in plant

communities. Science, 147, 250–260.Wilson, J.B. (1991) Methods for fitting dominance/diversity

curves. Journal of Vegetation Science, 2, 35–46.

Journal of Biogeography 44, 1524–1536ª 2017 John Wiley & Sons Ltd

1535

Biogeographical assessment of myxomycete assemblages across the Tropics

Wrigley de Basanta, D., Stephenson, S.L., Lado, C., Estrada-

Torres, A. & Nieves-Rivera, A.M. (2008) Lianas as a

microhabitat for myxomycetes in tropical forests. Fungal

Diversity, 28, 109–125.Wrigley de Basanta, D., Lado, C., Estrada-Torres, A. &

Stephenson, S.L. (2009) Description and life cycle of a

new Didymium (Myxomycetes) from arid areas of Argen-

tina and Chile. Mycologia, 101, 707–716.Wrigley de Basanta, D., Lado, C., Estrada-Torres, A. &

Stephenson, S.L. (2010) Biodiversity of myxomycetes in

subantarctic forests of Patagonia and Tierra del Fuego,

Argentina. Nova Hedwigia, 90, 45–79.Wrigley de Basanta, D., Lado, C. & Estrada-Torres, A. (2012)

Description and life cycle of a new Physarum (Myx-

omycetes) from the Atacama Desert in Chile. Mycologia,

104, 1206–1212.

SUPPORTING INFORMATION

Additional Supporting Information may be found in the

online version of this article:

Appendix S1 Supplementary figures and tables.

Appendix S2 Collated database of the study areas.

Appendix S3 Input files used in R.

BIOSKETCH

Nikki Heherson A. Dagamac is broadly interested in bio-

geography and biodiversity of tropical myxomycetes. The

group worked for a number of decades on developing a bet-

ter understanding of the global distribution patterns, taxon-

omy and ecology of myxomycetes.

Author contributions: M.S. conceptualized and designed the

present study; data from the Neotropical region were taken

from surveys of M.S., Y.K.N., C.L., C.R. and S.L.S; data from

the Palaeotropical region originated from field surveys of

N.H.A.D., Y.K.N., T.E.D.C., M.U. and M.S; N.H.A.D. com-

piled all data from the eight surveys, assembled the initial spe-

cies lists and collated the dataset; N.H.A.D., M.U. and M.S.

performed the ecological analysis of the dataset and interpreted

the results; N.H.A.D. and M.S. prepared the manuscript, which

was approved by all authors and improved by Y.K.N., C.L. and

C.R. S.L.S. did the English correction of the text.

Editor: Len N. Gillman

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